Chromosome replication and segregation govern the biogenesis and inheritance of inorganic polyphosphate granules

Molecular Biology of the Cell

Volumn 24, Issue 20, 2013, Pages 3177-3186

  Henry, Jonathan T ^a   Crosson, Sean ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHOTRANSFERASE; POLYPHOSPHATE; POLYPHOSPHATE KINASE 1; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CAULOBACTER CRESCENTUS; CELL CYCLE; CELL CYCLE REGULATION; CELLULAR DISTRIBUTION; CHROMOSOME REPLICATION; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOLOGY; DAUGHTER CELL; ENZYME ACTIVE SITE; INHERITANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SYNTHESIS;

CATALYSIS; CATALYTIC DOMAIN; CAULOBACTER CRESCENTUS; CELL DIVISION; CHROMOSOME SEGREGATION; CHROMOSOMES; MICROSCOPY, ELECTRON; MULTIPROTEIN COMPLEXES; PHOSPHOTRANSFERASES (PHOSPHATE GROUP ACCEPTOR); POLYPHOSPHATES;

EID: 84885642867     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-04-0182     Document Type: Article

References (69)

1. Abramov AY, Fraley C, Diao CT, Winkfein R, Colicos MA, Duchen MR, French RJ, Pavlov E (2007). Targeted polyphosphatase expression alters mitochondrial metabolism and inhibits calcium-dependent cell death. Proc Natl Acad Sci USA 104, 18091-18096.
2. Ahn K, Kornberg A (1990). Polyphosphate kinase from Escherichia coli. Purification and demonstration of a phosphoenzyme intermediate. J Biol Chem 265, 11734-11739.
3. Arnold K, Bordoli L, Kopp J, Schwede T (2006). The SWISS-MODEL workspace: a Web-based environment for protein structure homology modelling. Bioinformatics 22, 195-201.
4. Aschar-Sobbi R, Abramov AY, Diao C, Kargacin ME, Kargacin GJ, French RJ, Pavlov E (2008). High sensitivity, quantitative measurements of polyphosphate using a new DAPI-based approach. J Fluoresc 18, 859-866.
5. Ausmees N, Jacobs-Wagner C (2003). Spatial and temporal control of differentiation and cell cycle progression in Caulobacter crescentus. Annu Rev Microbiol 57, 225-247.
6. Babeş V (1895). Beobachtungen über die metachromatischen Körperchen, Sporenbildung, Verzwiegung, Kolben- und Kapsel-bildung pathogener Bakterien. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg 20, 412-420.
7. Bernstein FC, Koetzle TF, Williams GJ, Meyer EF, Brice MD, Rodgers JR, Kennard O, Shimanouchi T, Tasumi M (1977). The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol 112, 535-542.
8. Blakemore R ( (1975). Magnetotactic bacteria. Science 190, 377-379.
9. Bode G, Mauch F, Ditschuneit H, Malfertheiner P (1993). Identification of structures containing polyphosphate in Helicobacter pylori. J Gen Microbiol 139, 3029-3033.
10. Boutte CC, Henry JT, Crosson S (2012). ppGpp and polyphosphate modulate cell cycle progression in Caulobacter crescentus. J Bacteriol 194, 28-35.
11. Breed RS, Bergey DH, Hitchens AP, Murray EGD (1948). Bergey's Manual of Determinative Bacteriology, Baltimore: Williams & Wilkins.
12. Cannon GC, Bradburne CE, Aldrich HC, Baker SH, Heinhorst S, Shively JM (2001). Microcompartments in prokaryotes: carboxysomes and related polyhedra. Appl Environ Microbiol 67, 5351-5361.
13. Collins TJ (2007). ImageJ for microscopy. Biotechniques 43, 25-30.
14. Comolli LR, Kundmann M, Downing KH (2006). Characterization of intact subcellular bodies in whole bacteria by cryo-electron tomography and spectroscopic imaging. J Microsc 223, 40-52.
15. Degnen ST, Newton A (1972). Dependence of cell division on the completion of chromosome replication in Caulobacter. J Bacteriol 110, 852-856.
16. Docampo R, de Souza W, Miranda K, Rohloff P, Moreno SNJ (2005). Acidocalcisomes-conserved from bacteria to man. Nat Rev Microbiol 3, 251-261.
17. Ely B (1991). Genetics of Caulobacter crescentus. Methods Enzymol 204, 372-384.
18. Fiebig A, Castro Rojas CM, Siegal-Gaskins D, Crosson S (2010). Interaction specificity, toxicity and regulation of a paralogous set of ParE/RelE-family toxin-antitoxin systems. Mol Microbiol 77, 236-251.
19. Fraley CD, Rashid MH, Lee SSK, Gottschalk R, Harrison J, Wood PJ, Brown MRW, Kornberg A (2007). A polyphosphate kinase 1 (ppk1) mutant of Pseudomonas aeruginosa exhibits multiple ultrastructural and functional defects. Proc Natl Acad Sci USA 104, 3526-3531.
20. Galan B, Dinjaski N, Maestro B, de Eugenio LI, Escapa IF, Sanz JM, Garcia JL, Prieto MA (2011). Nucleoid-associated PhaF phasin drives intracellular location and segregation of polyhydroxyalkanoate granules in Pseudomonas putida KT2442. Mol Microbiol 79, 402-418.
21. Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005). Protein identification and analysis tools on the ExPASy server. In: The Proteomics Protocols Handbook, ed. JM Walker, Totowa, NJ: Humana Press, 571-607.
22. Goley ED, Iniesta AA, Shapiro L (2007). Cell cycle regulation in Caulobacter: location, location, location. J Cell Sci 120, 3501-3507.
23. Gómez-García MR, Kornberg A (2004). Formation of an actin-like filament concurrent with the enzymatic synthesis of inorganic polyphosphate. Proc Natl Acad Sci USA 101, 15876-15880.
24. Gordon GS, Sitnikov D, Webb CD, Teleman A, Straight A, Losick R, Murray AW, Wright A (1997). Chromosome and low copy plasmid segregation in E. coli: visual evidence for distinct mechanisms. Cell 90, 1113-1121.
25. Harold FM (1966). Inorganic polyphosphates in biology: structure, metabolism, and function. Bacteriol Rev 30, 772-794.
26. Holmstrom KM, Marina N, Baev AY, Wood NW, Gourine AV, Abramov AY (2013). Signalling properties of inorganic polyphosphate in the mammalian brain. Nat Commun 4, 1362-1362.
27. Hwang LC, Vecchiarelli AG, Han Y-W, Mizuuchi M, Harada Y, Funnell BE, Mizuuchi K (2013). ParA-mediated plasmid partition driven by protein pattern self-organization. EMBO J 32, 1238-1249.
28. Iancu CV, Morris DM, Dou Z, Heinhorst S, Cannon GC, Jensen GJ (2010). Organization, structure, and assembly of alpha-carboxysomes determined by electron cryotomography of intact cells. J Mol Biol 396, 105-117.
29. Jagannathan V, Kaur P, Datta S (2010). Polyphosphate kinase from M. tuberculosis: an interconnect between the genetic and biochemical role. PLoS One 5, e14336.
30. Jensen TE (1968). Electron microscopy of polyphosphate bodies in a blue-green alga, Nostoc pruniforme. Arch Mikrobiol 62, 144-152.
31. Klebahn H (1895). Gasvakuolen, ein Bestandteil der Zellen der wasserblütenbildenden Phycochromaceen. Flora 80, 241-282.
32. Komeili A, Li Z, Newman DK, Jensen GJ (2006). Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311, 242-245.
33. Kulaev IS, Vagabov VM, Kulakovskaya TV (2004). The Biochemistry of Inorganic Polyphosphates, Chichester, England: John Wiley & Sons.
34. Kumble KD, Ahn K, Kornberg A (1996). Phosphohistidyl active sites in polyphosphate kinase of Escherichia coli. Proc Natl Acad Sci USA 93, 14391-14395.
35. Kuroda A, Nomura K, Ohtomo R, Kato J, Ikeda T, Takiguchi N, Ohtake H, Kornberg A (2001). Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 293, 705-708.
36. Lindner AB, Madden R, Demarez A, Stewart EJ, Taddei F (2008). Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105, 3076-3081.
37. Modell JW, Hopkins AC, Laub MT (2011). A DNA damage checkpoint in Caulobacter crescentus inhibits cell division through a direct interaction with FtsW. Genes Dev 25, 1328-1343.
38. Morrissey JH, Choi SH, Smith SA (2012). Polyphosphate: an ancient molecule that links platelets, coagulation, and inflammation. Blood 119, 5972-5979.
39. Motomura K, Takiguchi N, Ohtake H, Kuroda A (2006). Polyamines affect polyphosphate accumulation in Escherichia coli. J Environ Biotechnol 6, 41-46.
40. Nocek B, Kochinyan S, Proudfoot M, Brown G, Evdokimova E, Osipiuk J, Edwards AM, Savchenko A, Joachimiak A, Yakunin AF (2008). Polyphosphate- dependent synthesis of ATP and ADP by the family-2 polyphosphate kinases in bacteria. Proc Natl Acad Sci USA 105, 17730-17735.
41. Ogawa N, Tzeng CM, Fraley CD, Kornberg A (2000). Inorganic polyphosphate in Vibrio cholerae: genetic, biochemical, and physiologic features. J Bacteriol 182, 6687-6693.
42. Osley MA, Newton A (1977). Mutational analysis of developmental control in Caulobacter crescentus. Proc Natl Acad Sci USA 74, 124-128.
43. Pfeifer F (2012). Distribution, formation and regulation of gas vesicles. Nat Rev Microbiol 10, 705-715.
44. Pfeiffer D, Wahl A, Jendrossek D (2011). Identification of a multifunctional protein, PhaM, that determines number, surface to volume ratio, subcellular localization and distribution to daughter cells of poly(3-hydroxybutyrate), PHB, granules in Ralstonia eutropha H16. Mol Microbiol 82, 936-951.
45. Poindexter JS (1984). The role of calcium in stalk development and in phosphate acquisition in Caulobacter crescentus. Arch Microbiol 138, 140-152.
46. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, Comolli LR, Moerner WE, Shapiro L (2010). A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12, 791-798.
47. Quardokus EM, Brun YV (2002). DNA replication initiation is required for mid-cell positioning of FtsZ rings in Caulobacter crescentus. Mol Microbiol 45, 605-616.
48. Rao NN, Gómez-García MR, Kornberg A (2009). Inorganic polyphosphate: essential for growth and survival. Annu Rev Biochem 78, 605-647.
49. Rashid MH, Rumbaugh K, Passador L, Davies DG, Hamood AN, Iglewski BH, Kornberg A (2000). Polyphosphate kinase is essential for biofilm development, quorum sensing, and virulence of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 97, 9636-9641.
50. Roberts MAJ, Wadhams GH, Hadfield KA, Tickner S, Armitage JP (2012). ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proc Natl Acad Sci USA 109, 6698-6703.
51. Savage DF, Afonso B, Chen AH, Silver PA (2010). Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327, 1258-1261.
52. Shively JM, Ball F, Brown DH, Saunders RE (1973). Functional organelles in prokaryotes: polyhedral inclusions (carboxysomes) of Thiobacillus neapolitanus. Science 182, 584-586.
53. Sinha NK, Snustad DP (1972). Mechanism of inhibition of deoxyribonucleic acid synthesis in Escherichia coli by hydroxyurea. J Bacteriol 112, 1321-1324.
54. Sliusarenko O, Heinritz J, Emonet T, Jacobs-Wagner C (2011). High-throughput, subpixel precision analysis of bacterial morphogenesis and intracellular spatio-temporal dynamics. Mol Microbiol 80, 612-627.
55. Stubbe J, Tian J, He A, Sinskey AJ, Lawrence AG, Liu P (2005). Nontemplate-dependent polymerization processes: polyhydroxyalkanoate synthases as a paradigm. Annu Rev Biochem 74, 433-480.
56. Sureka K, Dey S, Datta P, Singh AK, Dasgupta A, Rodrigue S, Basu J, Kundu M (2007). Polyphosphate kinase is involved in stress-induced mprAB-sigE-rel signalling in mycobacteria. Mol Microbiol 65, 261-276.
57. Takade A, Umeda A, Misumi T, Sawae Y, Amako K (1991). Accumulation of phosphate-containing granules in the nucleoid area of Pseudomonas aeruginosa. Microbiol Immunol 35, 367-374.
58. Thanbichler M, Shapiro L (2006). MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126, 147-162.
59. Tocheva EI, Matson EG, Morris DM, Moussavi F, Leadbetter JR, Jensen GJ (2011). Peptidoglycan remodeling and conversion of an inner membrane into an outer membrane during sporulation. Cell 146, 799-812.
60. Tomasz M (1995). Mitomycin C: small, fast and deadly (but very selective). Chem Biol 2, 575-579.
61. Toro E, Hong S-H, McAdams HH, Shapiro L (2008). Caulobacter requires a dedicated mechanism to initiate chromosome segregation. Proc Natl Acad Sci USA 105, 15435-15440.
62. van Veen HW, Abee T, Kortstee GJ, Pereira H, Konings WN, Zehnder AJ (1994). Generation of a proton motive force by the excretion of metal-phosphate in the polyphosphate-accumulating Acinetobacter johnsonii strain 210A. J Biol Chem 269, 29509-29514.
63. Viollier PH, Thanbichler M, McGrath PT, West L, Meewan M, McAdams HH, Shapiro L (2004). Rapid and sequential movement of individual chromosomal loci to specific subcellular locations during bacterial DNA replication. Proc Natl Acad Sci USA 101, 9257-9262.
64. Voelz H, Voelz U, Ortigoza RO (1966). The "polyphosphate overplus" phenomenon in Myxococcus xanthus and its influence on the architecture of the cell. Arch Mikrobiol 53, 371-388.
65. Wadhams GH, Martin AC, Porter SL, Maddock JR, Mantotta JC, King HM, Armitage JP (2002). TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol Microbiol 46, 1211-1221.
66. Werner JN, Chen EY, Guberman JM, Zippilli AR, Irgon JJ, Gitai Z (2009). Quantitative genome-scale analysis of protein localization in an asymmetric bacterium. Proc Natl Acad Sci USA 106, 7858-7863.
67. Wortinger M, Sackett MJ, Brun YV (2000). CtrA mediates a DNA replication checkpoint that prevents cell division in Caulobacter crescentus. EMBO J 19, 4503-4512.
68. Zhang H, Gómez-García MR, Shi X, Rao NN, Kornberg A (2007). Polyphosphate kinase 1, a conserved bacterial enzyme, in a eukaryote, Dictyostelium discoideum, with a role in cytokinesis. Proc Natl Acad Sci USA 104, 16486-16491.
69. Zhu Y, Huang W, Lee SSK, Xu W (2005). Crystal structure of a polyphosphate kinase and its implications for polyphosphate synthesis. EMBO Rep 6, 681-687.